Evidence for a rhesus monkey model of asymptomatic tuberculosis

Journal of Medical Primatology

Volumn 33, Issue 3, 2004, Pages 134-145

  Gormus, Bobby J ^a   Blanchard, James L ^a   Alvarez, Xavier H ^a   Didier, Peter J ^a  

^a TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

Author keywords

Histopathology; Skin test

Indexed keywords

BACTERIAL PROTEIN; GAMMA INTERFERON; INTERLEUKIN 4; LIPOARABINOMANNAN; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; BACTERIAL STRAIN; BACTERIUM CULTURE; COLONY FORMING UNIT; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE MODEL; GENETIC CODE; HISTOPATHOLOGY; IN VITRO STUDY; INOCULATION; LUNG ALVEOLUS CELL; LUNG LAVAGE; LUNG TUBERCULOSIS; LYMPHOCYTE TRANSFORMATION; MALE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PATHOGENESIS; PERIPHERAL BLOOD MONONUCLEAR CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RHESUS MONKEY; STATISTICAL SIGNIFICANCE; SYMPTOMATOLOGY;

ANIMALS; BODY BURDEN; BRONCHOALVEOLAR LAVAGE FLUID; CYTOKINES; DISEASE MODELS, ANIMAL; DNA; DNA PRIMERS; ELECTROPHORESIS, AGAR GEL; ENZYME-LINKED IMMUNOSORBENT ASSAY; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; IMMUNOHISTOCHEMISTRY; IMMUNOSUPPRESSION; LEUKOCYTES, MONONUCLEAR; LIPOPOLYSACCHARIDES; LYMPHOCYTE ACTIVATION; MACACA MULATTA; MICROSCOPY, CONFOCAL; MYCOBACTERIUM TUBERCULOSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TIME FACTORS; TUBERCULOSIS;

ANIMALIA; MACACA MULATTA; MYCOBACTERIUM; MYCOBACTERIUM TUBERCULOSIS;

EID: 2442611029     PISSN: 00472565     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-0684.2004.00062.x     Document Type: Article

References (48)

1. Anacker RL, Brehmer W, Barclay WR, Leif WR, Ribi E, Simmons JH, Smith AW: Superiority of intravenously administered BCG and BCG cell walls in protecting rhesus monkeys (Macaca mulatta) against airborne tuberculosis. Z Immunitatsforsch Exp Klin Immunol 143:363-376, 1972.
2. Appelberg R, Castro AG, Pedrosa J, Silva RA, Orme IM, Minoprio P: Role of gamma interferon and tumor necrosis factor alpha during T-cell-independent and -dependent phases of Mycobacterium avium infection [published erratum appears in Infect Immun 1995 Mar; 63(3):1145]. Infect Immun 62:3962-3971, 1994.
3. Barclay WR, Anacker RL, Brehmer W, Leif W, Ribi E: Aerosol-induced tuberculosis is subhuman primates and the course of the disease after intravenous BCG vaccination. Infect Immun 2:574-582, 1970.
4. Barclay WR, Busey WM, Dalgard DW, Good RC, Janicki BW, Kasik JE, Ribi E, Ulrich CE, Wolinsky E: Protection of monkeys against airborne tuberculosis by aerosol vaccination with Bacillus Calmette-Guerin. Am Rev Respir Dis 107:351-358, 1973.
5. Barnes PF, Lu S, Abrams JS, Wang E, Yamamura M, Modlin RL: Cytokine production at the site of disease in human tuberculosis. Infect Immun 61:3482-3489, 1993.
6. Bekker LG, Moreira AL, Bergtold A, Freeman S, Ryffel B, Kaplan G: Immunopathologic effects of tumor necrosis factor alpha in murine mycobacterial infection are dose dependent. Infect Immun 68:6954-6961, 2000.
7. Benveniste O, Vaslin B, Villinger F, Le Grand R, Ansari AA, Dormont D: Cytokine mRNA levels in unmanipulated (ex vivo) and in vitro stimulated monkey PBMCs using a semi-quantitative RT-PCR and high sensitivity fluorescence-based detection strategy. Cytokine 8:32-41, 1996.
8. Bohm RP Jr, Dennis V, Blanchard JL, Philipp MT, Gerber MA: Clinical outcome of a protocol to produce immunosuppression in rhesus monkeys (Macaca mulatta): application to infectious disease and gene therapy studies (In Process Citation). J Med Primatol 28:344-352 (MEDLINE), 1999.
9. Capuano SV, Croix DA, Pawar S, Zinovik A, Myers A, Lin PL, Bissel S, Fuhrman C, Klein E, Flynn JL: Experimental Mycobacterium tuberculosis infection of cynomolgus macaques closely resembles the various manifestations of human M. tuberculosis infection. Infect Immun 71:5831-5844, 2003.
10. Chaparas SD, Good RC, Janicki BW: Tuberculin-induced lymphocyte transformation and skin reactivity in monkeys vaccinated or not vaccinated with Bacille Calmette-Guerin, then challenged with virulent Mycobacterium tuberculosis. Am Rev Respir Dis 112:43-47, 1975.
11. Cooper AM, Dalton DK, Stewart TA, Griffin JP, Russell DG, Orme IM: Disseminated tuberculosis in interferon gamma gene-disrupted mice. J Exp Med 178:2243-2247, 1993.
12. Dye C, Scheele S, Dolin R, Pathania G, Raviglione M: Global burden of tuberculosis. Estimated incidence, prevalence, and mortality by country. JAMA 282:677-686, 1999.
13. Flynn JL, Chan J: Immunology of tuberculosis. Annu Rev Immunol 19:93-129, 2001.
14. Flynn JL, Chan J: Tuberculosis: latency and reactivation. Infect Immun 69:4195-4201, 2001.
15. Flynn JL, Chan J, Triebold KJ, Dalton DK, Stewart TA, Bloom BR: An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J Exp Med 178:2249-2254, 1993.
16. Flynn JL, Goldstein MM, Chan J, Triebold KJ, Pfeffer K, Lowenstein CJ, Schreiber R, Mak TW, Bloom BR: Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity 2:561-572, 1995.
17. Giambartolomei GH, Lasater BL, Villinger F, Dennis VA: Diminished production of T helper 1 cytokines and lack of induction of IL-2R+ T cells correlate with T-cell unresponsiveness in rhesus monkeys chronically infected with Brugia malayi. Exp Parasitol 90:77-85, 1998.
18. Githui WA, Wilson SM, Drobniewski FA: Specificity of IS6110-based DNA fingerprinting and diagnostic techniques for Mycobacterium tuberculosis complex. J Clin Microbiol 37:1224-1226, 1999.
19. Glatman-Freedman A, Mednick AJ, Lendvai N, Casadevall A: Clearance and organ distribution of Mycobacterium tuberculosis lipoarabinomannan (LAM) in the presence and absence of LAM-binding immunoglobulin M. Infect Immun 68:335-341, 2000.
20. Good RC: Biology of the mycobacterioses. Simian tuberculosis: immunologic aspects. Ann N Y Acad Sci 154:200-213, 1968.
21. Good RC: Nonhuman Primates and Medical Research. New York: Academic Press, pp. 39-60.
22. Good RC: The Mycobacteria: A Source Book, Part B. New York: Marcel Dekker, Inc., pp. 903-924.
23. Good RC, McCarroll NE: Mycobacterial Infections of Zoo Animals. Washington, DC: Smithsonian Institution Press, pp. 115-121.
24. Gormus BJ, Baskin GB, Xu K, Ratterree MS, Martin LN, Mack PA, Bohm RP, Meyers WM, Walsh GP: Antileprosy protective vaccination of rhesus monkeys with BCG or BCG plus heat-killed Mycobacterium leprae: immunologic observations. Int J Lepr Other Mycobact Dis 68:27-39, 2001.
25. Gormus BJ, Murphey-Corb M, Martin LN, Baskin GB, Mack PA, Xu K, Ratteree MS, Gerone PJ, Scollard DM, Gillis TP: Impaired responses to Mycobacterium leprae antigens in rhesus monkeys experimentally inoculated with simian immunodeficiency virus and M. leprae. Lepr Rev 69:24-39, 1998.
26. Gormus BJ, Xu K, Baskin GB, Martin LN, Bohm RP Jr, Blanchard JL, Mack PA, Ratterree MS, Meyers WM, Walsh GP: Experimental leprosy in rhesus monkeys: transmission, susceptibility, clinical and immunological findings. Lepr Rev 69:235-245, 1998.
27. Gormus BJ, Xu K, Cho SN, Baskin GB, Bohm RP, Martin LN, Blanchard JL, Mack PA, Ratterree MS, Meyers WM, Walsh GP: Experimental leprosy in monkeys: II. Longitudinal serological observations in sooty mangabey monkeys. Lepr Rev 66:105-125, 1995.
28. Gormus BJ, Xu K, Meyers WM, Walsh GP, Levis WR, Meeker HC: Antibodies to lipoarabinomannan antigen in sooty mangabey monkeys experimentally inoculated with Mycobacterium leprae. Int J Lepr Other Mycobact Dis 58:65-72, 1990.
29. Hernandez-Pando R, Pavon L, Arriaga K, Orozco H, Madrid-Marina V, Rook G: Pathogenesis of tuberculosis in mice exposed to low and high doses of an environmental mycobacterial saprophyte before infection. Infect Immun 65:3317-3327, 1997.
30. Janicki BW, Good RC, Minden P, Affronti LF, Hymes WF: Immune responses in rhesus monkeys after Bacillus Calmette-Guerin vaccination and aerosol challenge with Mycobacterium tuberculosis. Am Rev Respir Dis 107:359-366, 1973.
31. Juffermans NP, Verbon A, Belisle JT, Hill PJ, Speelman P, van Deventer SJ, van der Poll T: Mycobacterial lipoarabinomannan induces an inflammatory response in the mouse lung: a role for interleukin-1. Am J Respir Crit Care Med 162:486-489, 2001.
32. Juffermans NP, Verbon A, van Deventer SJH, van Deutekom H, Belisle JT, Ellis ME, Speelman P, van der Poll T: Elevated chemokine concentrations in sera of human immunodeficiency virus (HIV)-seropositive and HIV-seronegative patients with tuberculosis: a possible role for Mycobacterial lipoarabinomannan. Infect Immun 67:4295-4297, 1999.
33. Khoo KH, Tang JB, Chatterjee D: Variations in mannose-capped terminal arabinan motifs of lipoarabinomannans from clinical isolates of Mycobacterium tuberculosis and Mycobacterium avium complex. J Biol Chem 276:3863-3871, 2001.
34. Kindler V, Sappino AP, Grau GE, Piguet PF, Vassali P: The inducing role of tumor necrosis factor in the development of bactericidal granulomas during BCG infection. Cell 56:731-740, 1989.
35. Langermans JAM, Andersen P, van Soolingen D, Vervenne RAW, Frost PA, van der Laan T, van Pinxteren AH, van den Hombergh J, Kroon S, Peekel I, Florquin S, Thomas AW: Divergent effect of Bacillus Calmette-Guerin (BCG) vaccination on Mycobacterium tuberculosis infection in highly related macaque species: implications for primate models in tuberculosis vaccine research. Proc Natl Acad Sci U S A 98:11497-11502, 2001.
36. Law KF, Jagirdar J, Weiden MD, Bodkin M, Rom WN: Tuberculosis in HIV-positive patients: cellular response and immune activation in the lung. Am J Respir Crit Care Med 153:1377-1384, 1996.
37. Lin Y, Zhang M, Hofman FM, Gong J, Barnes PF: Absence of a prominent Th2 cytokine response in human tuberculosis. Infect Immun 64:1351-1356, 1996.
38. McMurray DN: A nonhuman primate model for pre-clinical testing of new tuberculosis vaccines. Clin Infect Dis 30 (Suppl. 3):210-212, 2002.
39. Mohan VP, Scanga CA, Tanaka KE, Tsang E, Tsai MC, Flynn JL, Chan J: Effects of tumor necrosis factor alpha on host immune response in chronic persistent tuberculosis: possible role for limiting pathology. Infect Immun 69:1847-1855, 2001.
40. Ribi E, Anacker RL, Barclay WR, Brehmer W, Harris SC, Leif WR, Simmons J: Efficacy of mycobacterial cell walls as a vaccine against airborne tuberculosis in the rhesus monkey. J Infect Dis 123:527-538, 1971.
41. Robinson DS, Ying S, Taylor IK, Wangoo A, Mitchell DM, Kay AB, Hamid Q, Shaw RJ: Evidence for a Th1-like bronchoalveolar T-cell subset and predominance of interferon-gamma gene activation in pulmonary tuberculosis. Am J Respir Crit Care Med 149:989-993, 1994.
42. Safi H, Gormus BJ, Didier PJ, Blanchard JL, Lakey DL, Martin LN, Murphey-Corb M, Vankayalapati R, Barnes PF: Spectrum of manifestations of Mycobacterium tuberculosis infection in primates infected with SIV. AIDS Res Hum Retroviruses 19:585-595, 2003.
43. Scanga CA, Mohan VP, Yu K, Joseph H, Tanaka K, Chan J, Flynn JL: Depletion of CD4(+) T cells causes reactivation of murine persistent tuberculosis despite continued expression of interferon gamma and nitric oxide synthase 2. J Exp Med 2000 (Aug 7) 192:347-358, 2001.
44. Schwander SK, Torres M, Sada E, Carranza C, Ramos E, Tary-Lehmann M, Wallis RS, Sierra J, Rich EA: Enhanced responses to Mycobacterium tuberculosis antigens by human alveolar lymphocytes during active pulmonary tuberculosis. J Infect Dis 178:1434-1445, 1998.
45. Villinger F, Brar SS, Mayne A, Chikkala N, Ansari AA: Comparative sequence analysis of cytokine genes from human and nonhuman primates. J Immunol 155:3946-3954, 1995.
46. Villinger F, Hunt D, Mayne A, Vuchetich M, Findley H, Ansari AA: Qualitative and quantitative studies of cytokines synthesized and secreted by non-human primate peripheral blood mononuclear cells. Cytokine 5:469-479, 1993.
47. Walsh GP, Tan EV, dela Cruz EC, Abalos RM, Villahermosa LG, Young LJ, Cellona RV, Nazareno JB, Horwitz MA: The Philippine cynomolgus monkey (Macaca fasicularis) provides a new nonhuman primate model of tuberculosis that resembles human disease. Nat Med 2:430-436, 1996.
48. Williams KC, Schwartz AJ, Corey S, Orandle MS, Kennedy W, Thompson B, Alvarez X, Brown C, Gartner S, Lackner AA: Proliferating cellular nuclear antigen expression as a marker of perivascular macrophages in simian immunodeficiency virus encephalitis. Am J Pathol 161:575-590, 2002.